Post–COVID-19 Acute Disseminated in a 17-Month-Old Loren A. McLendon, MD,a,b Chethan K. Rao, DO, MS,a,b Cintia Carla Da Hora, MD,c Florinda Islamovic, MD,c Fernando N. Galan, MDb

Neurologic manifestations of severe acute respiratory syndrome coronavirus abstract 2 (SARS-CoV-2) infection in pediatric patients have been reported in the acute and postinfectious stages of coronavirus disease 2019. Acute disseminated encephalomyelitis (ADEM) typically presents in children after a viral illness at a mean age of 3 to 7 years. A total of 60% to 90% of literature-reported pediatric patients with ADEM have minimal to no neurologic deficits at long- term follow-up. We present a 17-month-old developmentally typical girl with aDivision of Child and Adolescent Neurology, Mayo Clinic parental complaints of irritability, upper extremity weakness, and gait College of Medicine and Science, Jacksonville, Florida; disturbance. She presented to the hospital afebrile and irritable with right- bDivision of Pediatric Neurology, Nemours Children Specialty Clinic, Jacksonville, Florida; and cDepartment of Pediatrics, sided nasolabial fold flattening, neck stiffness, left upper extremity rigidity, College of Medicine - Jacksonville, University of Florida, right upper extremity paresis, bilateral lower extremity hyperreflexia, and Jacksonville, Florida truncal . During her hospital course, she became somnolent with Dr McLendon performed data acquisition, drafted autonomic instability and was transferred to intensive care. Contrasted brain the initial manuscript, revised the figure, and MRI revealed diffuse patchy T2 hyperintensities without contrast critically reviewed the manuscript; Dr Rao performed data acquisition, contributed to the enhancement. Nasopharyngeal SARS-CoV-2 polymerase chain reaction and drafting of the initial manuscript and figure, and serum antibody testing results were positive. Cerebral spinal fluid analysis critically reviewed the manuscript; Drs Da Hora and was unremarkable. Respiratory viral panel and autoimmune encephalitis and Islamovic performed data acquisition and contributed to the drafting of the initial manuscript; demyelinating disorders panel results were negative. She was started on high- Dr Galan conceptualized the study, supervised data dose methylprednisolone and intravenous immunoglobulin, with collection, and critically reviewed the manuscript; improvement in mental status, focal deficits, and ambulation. After hospital and all authors approved the final manuscript as submitted and agree to be accountable for all discharge, she received inpatient rehabilitation for 2 weeks and at 2 month aspects of the work. follow-up had a full neurologic recovery. We report the youngest case of DOI: https://doi.org/10.1542/peds.2020-049678 postinfectious ADEM due to SARS-CoV-2 in a toddler. Early recognition of Accepted for publication Mar 18, 2021 autoimmune and inflammatory complications of SARS-CoV-2 is vital for early Address correspondence to Fernando N. Galan, MD, aggressive immunomodulatory treatment and, consequently, improved Division of Child Neurology, Nemours Children morbidity in these patients. Specialty Care, 807 Children’s Way, Jacksonville, FL 32207. E-mail: [email protected] PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Coronavirus disease 2019 (COVID-19) multisystem inflammatory syndrome, Copyright © 2021 by the American Academy of caused by the novel coronavirus severe and a variety of neurologic sequelae.2 Pediatrics acute respiratory syndrome Individual cases of seizure, FINANCIAL DISCLOSURE: The authors have indicated coronavirus 2 (SARS-CoV-2) cerebrovascular infarction, encephalitis, they have no financial relationships relevant to this disproportionately spares pediatric and myelitis in children with active or article to disclose. populations, representing ,2% of recent COVID-19 infection have been FUNDING: No external funding. 2,3 reported cases in multinational reported. POTENTIAL CONFLICT OF INTEREST: The authors have studies.1 Up to 35% of infected children indicated they have no potential conflicts of interest are asymptomatic, and the remainder Acute disseminated encephalomyelitis to disclose. often have mild symptoms, such as (ADEM), or postinfectious fever, cough, and headache. However, encephalomyelitis, is an immune-mediated To cite: McLendon LA, Rao CK, Da Hora CC, et al. severe complications related to COVID- process marked by demyelination and Post–COVID-19 Acute Disseminated – 19 in children have been reported, multifocal neurologic manifestations.4 6 Encephalomyelitis in a 17-Month-Old. Pediatrics. 2021;147(6):e2020049678 including respiratory failure, ADEM is typically preceded by symptoms

Downloaded from www.aappublications.org/news by guest on September 29, 2021 PEDIATRICS Volume 147, number 6, June 2021:e2020049678 CASE REPORT of fever, malaise, vomiting, and/or difficulty feeding herself, walking, and revealed multifocal hyperintense headaches. Neurologic symptoms are sitting without support. She T2 fluid-attenuated inversion multifocal and correlate with presented to the hospital with recovery (FLAIR) signals in bilateral radiologic lesions in the brain and/or parental complaints symptoms of subcortical and periventricular white spinal cord, clinically presenting as irritability, weakness of upper matter without contrast enhancement ataxia, encephalopathy, hemiplegia, extremities, and gait disturbance. She (Fig 1). hemiparesthesias, visual changes, was found to be afebrile but irritable, seizures, or cranial nerve palsies.4,5,7,8 with subtle right-sided nasolabial fold An MRI of the whole spine without This neurologic decline occurs rapidly flattening, significant neck stiffness contrast was unremarkable. Cerebral within days to weeks after the with a positive Brudzinski’s sign, left spinal fluid (CSF) and serum studies prodromal illness; symptoms in the upper extremity rigidity, right upper were performed before the initiation majority of patients do not progress extremity paresis, bilateral lower of high-dose methylprednisolone. CSF beyond 3 months.9 We present a case extremity hyperreflexia, and truncal analysis revealed mild pleocytosis of ADEM secondary to COVID-19 in ataxia. with lymphocytic predominance: 5 a 17-month-old girl who fared well per mcL white blood cells (81% with early and aggressive In the initial evaluation, an lymphocytes, 19% monocytes), 1 per immunomodulating therapy, which electrocardiogram was included, with mcL red blood cell, glucose of 58 mg/ included high-dose corticosteroids normal sinus rhythm, possible right dL, and protein of 17 mg/dL. The CSF and intravenous immunoglobin atrium enlargement, and left had zero oligoclonal bands, with (IVIG) treatments. ventricular hypertrophy. A a normal (IgG) transthoracic echocardiogram index and IgG synthesis rate. The CSF performed in the PICU was normal. polymerase chain reaction (PCR) was CASE Laboratory evaluation noted elevated negative for enterovirus. Other A 17-month-old African American, inflammatory markers, including an infectious studies were not obtained, non-Hispanic, previously healthy, and erythrocyte sedimentation rate of given the limited CSF sample. Serum developmentally typical girl 25 mm/hour, which increased to study results for antinuclear antibody, presented to the emergency 40 mm/hour within 2 days, and Aquaporin 4 antibodies, myelin department with , lactate dehydrogenase of 406 IU/L. oligodendrocyte glycoprotein (MOG) progressively worsening weakness, Normal serum studies included antibodies, and thyroid peroxidase and unsteady gait. She had 5 days of complete blood count, comprehensive antibodies were negative. CSF and fever, ∼13 days before presentation, metabolic panels, prothrombin time serum bacterial culture results were with a maximum temperature of and international normalized ratio, negative. An upper respiratory viral 38.9°C without associated upper partial thromboplastin time, ferritin, PCR panel via nasopharyngeal swab respiratory or gastrointestinal D-dimer, brain natriuretic peptide, and a stool PCR were negative for symptoms. After fever resolution, her troponins, ammonia levels, and enterovirus and rotavirus antigen. parents noticed progressive fatigue, creatine kinase. An MRI of the brain Results from a SARS-CoV-2 PCR via decreased communication, and with and without gadolinium contrast nasopharyngeal swab and serum

FIGURE 1 A, An MRI brain T2 FLAIR axial image revealing diffuse hyperintensities in the subcortical white matter. B, An MRI brain T2 axial image revealing diffuse patchy T2 hyperintensities. C, An MRI brain T2 FLAIR coronal image revealing hyperintensities in the cortical and subcortical white matter.

Downloaded from www.aappublications.org/news by guest on September 29, 2021 2 MCLENDON et al SARS-CoV IgG antibody testing were postinfectious sequelae have included converting enzyme 2 receptors both positive. Infection was evaluated Guillain-Barre syndrome and ADEM. required for viral cell entry into brain by using Hologic Aptima SARS-CoV-2 Neurologic manifestations in endothelium.22 COVID-19 cases have assay (sensitivity: .90%) and serum pediatric populations mimic those been exceedingly low in pediatric SARS-CoV IgG antibody (sensitivity: seen in adult populations but also populations, but cases of serious 84%; specificity: 100%) testing include febrile seizures, acute flaccid neurologic manifestations have been performed by Abbott myelitis, and a single pediatric report reported in isolated cases.2,3,23,24 Kim Laboratories.10,11 The patient’s of ADEM in an adolescent.2,3 et al25 recently proposed that parents were health care workers. pediatric populations may be less Her father tested positive for SARS- ADEM is an autoimmune disorder of susceptible to neurologic CoV-2 3 months before the patient’s the (CNS), complications of SARS-CoV-2 because presentation. with suspected pathogenesis from angiotensin-converting enzyme 2 is activation of the immune system by expressed the lowest in younger On day 2 of hospitalization, she was environmental triggers, such as children. transferred to the PICU because of infection in genetically susceptible increased lethargy, autonomic individuals.14,15 Myelin autoantigens, Many other causes of encephalopathy instability, and concern for seizures. such as myelin basic protein, can mimic ADEM, and a complete Electroencephalography revealed proteolipid protein, and MOGs, are evaluation is indicated.26 diffuse slowing, consistent with implicated in the pathogenesis.15 Encephalopathy has a broad encephalopathy, but no seizures or These proteins share antigenic differential diagnosis and commonly epileptiform activity. Because of properties with those of an infectious results from an infectious agent, such clinical deterioration, IVIG 2 g/kg pathogen; this molecular mimicry as a virus, bacteria, or arthropod- divided over 4 days was initiated, in triggers an autoimmune response borne microorganism.6,26 If the CSF addition to completion of a 5 day leading to demyelination of the reveals nonspecific abnormalities and course of high-dose IV CNS.14 Antiviral antibodies or a cell- there is evidence of white matter methylprednisolone (30 mg/kg mediated response to these lesions on an MRI, other per day). pathogens can cross-react with the inflammatory demyelinating myelin antigens, leading to disorders should be considered.17,27 On day 5 of hospitalization, she was 14–16 transferred to the general pediatric ADEM. Common demyelinating disorders in floor. Her examination continued to children include: In North America, the estimated (MS), MOG antibody-associated improve. She was alert, attentive to incidence of ADEM is 0.2 to 0.4 per the examiner, able to sit unsupported, disease, neuromyelitis optica 100 000 per year in pediatric spectrum disorder, and clinically and able to walk with support. She patients.5,17 ADEM is primarily seen was discharged to inpatient isolated syndromes (, in children, between 3 and 7 years , and brainstem rehabilitation for 2 weeks, with a 6- 6,18,19 old, and young adults. There is encephalitis).17,27 week oral prednisone taper. A a boy to girl predominance of 1 to neurologic examination at 2 month 0.8.7 It is frequently associated with In pediatric patients, demyelinating postdischarge neurology follow-up infections and recent immunization. disease etiologies can be difficult to had completely normalized. In 64% to 93% of ADEM cases, stratify because many of the initial a preceding infection was presentations overlap among disease 4,5,7,8,20 DISCUSSION identified. In adults, COVID- and syndromes. Among patients 19–associated encephalopathy has initially diagnosed with ADEM, ∼50% There is a growing body of evidence been reported in up to 37% of some were found to have MOG antibodies, of neurologic sequelae secondary to infected cohorts, but the etiology has whereas aquaporin-4 antibodies COVID-19 disease. Common varied among toxic-metabolic, traditionally associated with neurologic symptoms during an seizures, , and neuromyelitis optica spectrum active infection include headache, potentially direct infection.21 disorder are rarer in children.28 MOG anosmia, and myalgias. Severe active antibody–positive spectrum disease is COVID-19 disease has been The proposed mechanisms of typically monophasic; however, associated with viral neuroinvasion include trans-synaptic persistent presence of antibodies has , hypoxic transmission retrograde from been associated with relapsing ischemic encephalopathy, acute peripheral nerve terminals to CNS disease.29,30 cerebrovascular insults, and acute tissues as in other coronaviruses. necrotizing hemorrhagic SARS-CoV-2 spreads across the Children appropriately diagnosed encephalopathy.12,13 Additional blood–brain barrier via angiotensin- with ADEM infrequently progress to

Downloaded from www.aappublications.org/news by guest on September 29, 2021 PEDIATRICS Volume 147, number 6, June 2021 3 meet the criteria for MS.28,31 At the initiation. Many children diagnosed COVID-19 in children based on US state time of presentation, our patient did with ADEM have a full recovery.27,34 health department data. Pediatrics. not meet the revised 2017 McDonald 2020;146(6):e2020027425 32 criteria for MS. Moreover, the CONCLUSIONS 2. Christy A. COVID-19: a review for the incidence of MS is rare in children pediatric neurologist. J Child Neurol. ,12 years of age.33 At 2-month follow- ADEM with typical neuroimaging 2020;35(13):934–939 findings of scattered T2 up, our patient had returned to 3. de Miranda Henriques-Souza AM, de hyperintensities primarily affecting baseline, with a nonfocal neurologic Melo ACMG, de Aguiar Coelho Silva the deep white matter can potentially examination. We do recognize that her Madeiro B, Freitas LF, Rocha-Filho PAS, follow-up interval was limited in occur after COVID-19 infection in Gonçalves FG. Acute disseminated duration but followed the typical toddlers. Immunomodulatory encephalomyelitis in a COVID-19 clinical course for ADEM. Additionally, treatment with high-dose IV pediatric patient. Neuroradiology. 2021; given our patient’s resolution of focal methylprednisolone and IVIG was 63(1):141–145 effective in this case, with a full deficits, reimaging was deferred to 4. Jayakrishnan MP, Krishnakumar P. limit exposure to sedation. neurologic recovery noted at 12 weeks, Clinical profile of acute disseminated although the follow-up duration was encephalomyelitis in children. J Pediatr Further consideration in the limited. Health care providers should Neurosci. 2010;5(2):111–114 differential diagnosis of ADEM consider ADEM when evaluating 5. Leake JAD, Albani S, Kao AS, et al. Acute includes other infectious and a child with encephalopathy and disseminated encephalomyelitis in autoimmune causes. Acute viral fi neurologic de cits after recovering childhood: epidemiologic, clinical and encephalitis was considered in our from COVID-19. laboratory features. Pediatr Infect Dis J. patient but thought to be less likely 2004;23(8):756–764 because she was afebrile on ACKNOWLEDGMENTS admission. Screening respiratory viral 6. Murthy SNK, Faden HS, Cohen ME, Bakshi R. Acute disseminated panel and CSF culture results were We thank the parents who provided encephalomyelitis in children. negative. The patient was unlikely to consent to include their child in the Pediatrics. 2002;110(2):e21 have had an active SARS-CoV-2 medical literature. Additionally, we infection at presentation, given the thank Dr Harry Abram for his help 7. Pavone P, Pettoello-Mantovano M, Le time line of parental exposure and the with diagnosis and management of Pira A, et al. 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Downloaded from www.aappublications.org/news by guest on September 29, 2021 PEDIATRICS Volume 147, number 6, June 2021 5 Post−COVID-19 Acute Disseminated Encephalomyelitis in a 17-Month-Old Loren A. McLendon, Chethan K. Rao, Cintia Carla Da Hora, Florinda Islamovic and Fernando N. Galan Pediatrics 2021;147; DOI: 10.1542/peds.2020-049678 originally published online March 24, 2021;

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Downloaded from www.aappublications.org/news by guest on September 29, 2021 Post−COVID-19 Acute Disseminated Encephalomyelitis in a 17-Month-Old Loren A. McLendon, Chethan K. Rao, Cintia Carla Da Hora, Florinda Islamovic and Fernando N. Galan Pediatrics 2021;147; DOI: 10.1542/peds.2020-049678 originally published online March 24, 2021;

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